Abstract
Seagrass meadows are highly productive habitats that support commercially and ecologically important fishes and invertebrates. However, evidence of fish-habitat relationships are seldom drawn from forereef seagrass meadows that are structurally simple in terms of species richness and relative size and, consequently, their role as habitats is unclear. In this study, fish-habitat relationships were examined in such meadows in the forereef seagrasses of Tinggi Island and Babi Besar Island, Malaysia, by documenting habitat complexity attributes (canopy height, shoot density and percent cover), distance to adjacent coral reefs, and water depth within 2×2 m quadrats. Fish assemblages were recorded using the Remote Underwater Video Station method. A total of 1166 individuals from 86 taxa were found and enumerated. This study showed that (1) fish density and species richness were significantly associated with seagrass percent cover alone; (2) commercially important carnivores formed the majority of the fish populations in the meadows, and (3) fish density and species richness were positively correlated with distance to the nearest adjacent coral reef, indicating the need to account for the effects of neighboring habitats in studies of this nature. Thus, structurally simple seagrass meadows are still important fish habitats, especially as feeding grounds for commercially significant carnivores.
About the authors
Nina Ann Jin Ho is a postgraduate student in University of Malaya. She received her early training in marine science from Borneo Marine Research Institute, University of Malaysia Sabah. She is a marine ecologist with working experience in marine tourism and conservation at Semporna Priority Conservation Area, Sulu-Sulawesi Marine Ecoregion. After years of working in the field, she has developed a special interest in reef fish ecology and fish habitat preferences in seagrass and coral reefs.
Jillian Lean Sim Ooi teaches at the Department of Geography, University of Malaya. She has a PhD in seagrass biogeography from the University of Western Australia for her work on the spatial patterns and processes of seagrass in Johor, Malaysia. Her current focus is on understanding how these meadows function as habitats for fish and as feeding grounds for dugongs and invertebrates.
Yang Amri Affendi is a research officer in the Institute of Ocean and Earth Sciences (IOES) and prior to that was teaching young padawans the arts of coral reef ecology in the Institute of Biological Sciences (IBS), University of Malaya. Early in his career he submitted himself to the mud of mangrove ecology and then proceeded to dive into coral reef ecology, focusing on scleractinian coral ecophysiology. At present, he is trying to understand more of marine ecosystems connectivity and climate change impacts on scleractinian corals in the Johor Marine Parks, Malaysia.
Ving Ching Chong was a professor in the Institute of Biological Sciences (IBS) and former Head of Marine Connectivity Studies, Institute of Ocean and Earth Sciences (IOES), University of Malaya. He is currently a research associate in the IBS after his retirement in 2016. VCC has a wide interest in mangrove and marine fisheries ecology, with current interests in ecosystems connectivity and conservation, food webs and trophodynamics, climate change and anthropogenic effects on marine systems, and the exploitation of marine microorganisms for aquaculture.
Acknowledgments
We acknowledge the University of Malaya Research Grant (RG200-12SUS) and Postgraduate Research Grant (PG053-2013B) for support of fieldwork and research materials, and the Department of Marine Park Malaysia for the research permit (JLTM630-7Jld.4(21)). We thank Lau CM, Ng KC, Chong WW, Yip MY, Ong GM, A. Rahman, and F. Mohamed for assisting in the field sampling. Appreciation to Then AYH for comments on the manuscript.
References
Ajemian, M.J., J.J. Wetz, B. Shipley-Lozano and G.W. Stunz. 2015. Rapid assessment of fish communities on submerged oil and gas platform reefs using remotely operated vehicles. Fish. Res. 167: 143–155.10.1016/j.fishres.2015.02.011Search in Google Scholar
Akaike, H. 1973. Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika 60: 255–265.10.1093/biomet/60.2.255Search in Google Scholar
Akaike, H. 1981. Likelihood of A model and information criteria. J. Econom. 16: 3–14.10.1016/0304-4076(81)90071-3Search in Google Scholar
Allen, G., R. Steene, P. Humann and N. DeLoach. 2012. Reef fish: identification tropical Pacific. New World Publication, Jacksonville. pp. 457.Search in Google Scholar
Bacheler, N.M. and K.W. Shertzer. 2014. Estimating relative abundance and species richness from video surveys of reef fishes. Fish. Bull. 113: 15–26.10.7755/FB.113.1.2Search in Google Scholar
Barbosa, A.M., J.A. Brown, A. Jimenez-Valverde and R. Real. 2015. Model evaluation and analysis. Package modEvA. Accessed on 30 June 2015. https://cran.r-project.org/web/packages/modEvA/modEvA.pdf.Search in Google Scholar
Bartholomew, A., R. Diaz and G. Cicchetti. 2000. New dimensionless indices of structural habitat complexity: predicted and actual effects on a predator’s foraging success. Mar. Ecol. Prog. Ser. 206: 45–58.10.3354/meps206045Search in Google Scholar
Cappo, M., E.S. Harvey and M. Shortis. 2006. Counting and measuring fish with baited video techniques – an overview. Aust. Soc. Fish Biol. 1:101–114.Search in Google Scholar
Conn, P.B. 2011. An evaluation and power analysis of fishery independent reef fish sampling in the Gulf of Mexico and U.S. South Atlantic. NOAA Tech. Memo. NMFS-SEFSC-610.Search in Google Scholar
Den Hartog, C. and J. Kuo. 2006. Taxonomy and biogeography of seagrasses. In: (A.W.D. Larkum, R.J. Orth and C.M. Duarte, eds) Seagrasses: biology, ecology and conservation. Springer Dordrecht, Dordrecht. pp. 1–23.10.1007/1-4020-2983-7_1Search in Google Scholar
Dorenbosch, M., M. Grol, M. Christianen, I. Nagelkerken and G. van der Velde. 2005. Indo-Pacific seagrass beds and mangroves contribute to fish density and diversity on adjacent coral reefs. Mar. Ecol. Prog. Ser. 302: 63–76.10.3354/meps302063Search in Google Scholar
Duarte, C.M. 2000. Marine biodiversity and ecosystem services: an elusive link. J. Exp. Mar. Bio. Ecol. 250: 117–131.10.1016/S0022-0981(00)00194-5Search in Google Scholar
Duarte, C.M. 2002. The future of seagrass meadows. Environ. Conserv. 29: 192–206.10.1017/S0376892902000127Search in Google Scholar
Duarte, C.M. and H. Kirkman. 2001. Methods for the measurement of seagrass abudance and depth distribution. In: (F.T. Short, C.A. Short and R.G. Coles, eds) Global seagrass research methods. Elsevier Science B.V., Amsterdam. pp. 141–153.10.1016/B978-044450891-1/50008-6Search in Google Scholar
Ellis, D.M. and E.E. DeMartini. 1995. Evaluation of a video camera technique for indexing abundances of juvenile pink snapper, Pristipomoides filamentosus, and other Hawaiian insular shelf fishes. Fish. Bull. 93: 67–77.Search in Google Scholar
English, S., C.R. Wilkinson and V.J. Baker. 1994. Survey manual for tropical marine resources. Australian Institute of Marine Science (AIMS).Search in Google Scholar
Erftemeijer, P.L.A. and J. Stapel. 1999. Primary production of deep – water Halophila ovalis meadows. Aquat. Bot. 65: 71–82.10.1016/S0304-3770(99)00032-7Search in Google Scholar
Fox, J., S. Weisberg, D. Adler, D. Bates, G. Baud-Bovy, S. Ellison, D. Firth, M. Friendly, G. Gorjanc, S. Graves, R. Heiberger, R. Laboissiere, G. Monette, D. Murdoch, H. Nilsson, D. Ogle, B. Ripley, W. Venables, D. Winsemius, A. Zeileis and R-Core. 2015. Companion to applied regression. Package car. Accessed on 30 June 2015. https://cran.r-project.org/web/packages/car/car.pdf.Search in Google Scholar
Fox, J., S. Weisberg, M. Friendly, J. Hong, R. Anderson, D. Firth and S. Taylor. 2016. Effect displays for linear, generalized linear, and other models. Package effects. Accessed on 30 June 2015. https://cran.r-project.org/web/packages/effects/effects.pdf.Search in Google Scholar
Froese, R. and D. Pauly, editors. 2012. FishBase. World Wide Web electronic publication. Accessed on 30 July 2013. https://www.fishbase.org.Search in Google Scholar
Gledhill, C.T. 2001. Reef fish assemblages on Gulf of Mexico shelf-edge banks. Doctoral dissertation. University of South Alabama, Mobile, Alabama.Search in Google Scholar
Guisan, A. and N.E. Zimmermann. 2000. Predictive habitat distribution models in ecology. Ecol. Modell. 135: 147–186.10.1016/S0304-3800(00)00354-9Search in Google Scholar
Guisan, A., T.C. Edwards and T. Hastie. 2002. Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol. Modell. 157: 89–100.10.1016/S0304-3800(02)00204-1Search in Google Scholar
Gullström, M., M. Bodin, P.G. Nilsson and M.C. Öhman. 2008. Seagrass structural complexity and landscape configuration as determinants of tropical fish assemblage composition. Mar. Ecol. Prog. Ser. 363: 241–255.10.3354/meps07427Search in Google Scholar
Halford, A.R. and A.A. Thompson. 1994. Visual census surveys of reef fish. Long-term Monit. Gt. Barrier Reef. Vol. 3. Australian Institute of Marine Science (AIMS).Search in Google Scholar
Hemminga, M.A. and C.M. Duarte. 2000. Seagrass ecology. Cambridge University Press, Cambridge.10.1017/CBO9780511525551Search in Google Scholar
Hixon, M.A. and J.P. Beets. 1993. Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol. Monogr. 63: 77–101.10.2307/2937124Search in Google Scholar
Honda, K., Y. Nakamura, M. Nakaoka, W.H. Uy and M.D. Fortes. 2013. Habitat use by fishes in coral reefs, seagrass beds and mangrove habitats in the Philippines. PLoS One 8: e65735.10.1371/journal.pone.0065735Search in Google Scholar PubMed PubMed Central
Hori, M., T. Suzuki, Y. Monthum, T. Srisombat, Y. Tanaka, M. Nakaoka and H. Mukai. 2009. High seagrass diversity and canopy-height increase associated fish diversity and abundance. Mar. Biol. 156: 1447–1458.10.1007/s00227-009-1184-3Search in Google Scholar
Irving, A.D., J.E. Tanner and S.G. Gaylard. 2013. An integrative method for the evaluation, monitoring, and comparison of seagrass habitat structure. Mar. Pollut. Bull. 66: 176–184.10.1016/j.marpolbul.2012.10.017Search in Google Scholar PubMed
Jelbart, J.E., P.M. Ross and R.M. Connolly. 2007. Fish assemblages in seagrass beds are influenced by the proximity of mangrove forests. Mar. Biol. 150: 993–1002.10.1007/s00227-006-0419-9Search in Google Scholar
Kovalenko, K.E., S.M. Thomaz and D.M. Warfe. 2012. Habitat complexity: approaches and future directions. Hydrobiologia 685: 1–17.10.1007/s10750-011-0974-zSearch in Google Scholar
Kuo, J. and C. Den Hartog. 2007. Seagrass morphology, anatomy, and ultrastructure. In: Segrasses: biology, ecology and conservation. Springer, Dordrecht. pp. 51–87.10.1007/1-4020-2983-7_3Search in Google Scholar
Larkum, A.W.D., R.J. Orth and C.M. Duarte. 2006. Seagrasses : biology, ecology and conservation. Springer, Dordrecht. pp. 676.Search in Google Scholar
Malaysian Meteorological Department. 2016. http://www.met.gov.my (Accessed 22 August 2016).Search in Google Scholar
McCloskey, R.M. and R.K.F. Unsworth. 2015. Decreasing seagrass density negatively influences associated fauna. Peer J. 3: e1053.10.7717/peerj.1053Search in Google Scholar
McCoy, E.D. and S.S. Bell. 1991. Habitat structure: the evolution and diversification of a complex topic. In: (S. Bell, E. McCoy and H. Mushinsky, eds) Habitat structure. Springer, Dordrecht. pp. 3–27.10.1007/978-94-011-3076-9_1Search in Google Scholar
Mckenzie, L. 2003. Guidelines for the rapid assessment and mapping of tropical seagrass habitats. Department of Primary Industries. The State of Queensland.Search in Google Scholar
Mckenzie, L.J., S.J. Campbell and C.A. Roder. 2001. Seagrass-Watch : manual for mapping and monitoring seagrass resources by community (citizen) volunteers. 2nd edition. Townsville, Queensland.Search in Google Scholar
Moore, E.C. and K.A. Hovel. 2010. Relative influence of habitat complexity and proximity to patch edges on seagrass epifaunal communities. Oikos 119: 1299–1311.10.1111/j.1600-0706.2009.17909.xSearch in Google Scholar
Nagelkerken, I., G. van der Velde, M.W. Gorissen, G.J. Meijer, T. Van’t Hof and C. den Hartog. 2000. Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuar. Coast. Shelf Sci. 51: 31–44.10.1006/ecss.2000.0617Search in Google Scholar
Nagelkerken, I., S. Kleijnen, T. Klop, R. van den Brand, E. de la Morinière and G. van der Velde. 2001. Dependence of Caribbean reef fishes on mangroves and seagrass beds as nursery habitats: a comparison of fish faunas between bays with and without mangroves / seagrass beds. Mar. Ecol. Prog. Ser. 214: 225–235.10.3354/meps214225Search in Google Scholar
National Hydrographic Centre. 2013. Tide tables Malaysia 2013. Vol. 1. National Hydrographic Centre, Royal Malaysian Navy, Port Klang.Search in Google Scholar
National Hydrographic Centre. 2014. Tide tables Malaysia 2014. Vol. 1. National Hydrographic Centre, Royal Malaysian Navy, Port Klang.Search in Google Scholar
Nelder, J.A., R.J. Baker and R.W.M. Wedderburn. 1972. Generalized linear models. J. R. Stat. Soc. 135: 370–384.10.2307/2344614Search in Google Scholar
Nelson, J.S. 2006. Fishes of the World. 4th edition. Wiley, New York. pp. 601.Search in Google Scholar
Oksanen, J., F.G. Blanchet, R. Kindt, P. Legendre, P.R. Minchin, R.B.O. Hara, G.L. Simpson, P. Solymos and M.H.H. Stevens. 2014. Community ecology package. Package vegan. Accessed on 30 June 2015. https://cran.r-project.org/web/packages/vegan/vegan.pdf.Search in Google Scholar
Ooi, J.L.S., G.A. Kendrick, K.P. Van Niel and Y.A. Affendi. 2011a. Knowledge gaps in tropical Southeast Asian seagrass systems. Estuar. Coast. Shelf Sci. 92: 118–131.10.1016/j.ecss.2010.12.021Search in Google Scholar
Ooi, J.L.S., G.A. Kendrick and K.P. Van Niel. 2011b. Effects of sediment burial on tropical ruderal seagrasses are moderated by clonal integration. Cont. Shelf Res. 31: 1945–1954.10.1016/j.csr.2011.09.005Search in Google Scholar
Orth, R.J., T.I.M.J.B. Carruthers, W.C. Dennison, C.M. Duarte, W. James, K.L.H. Jr, A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, S. Olyarnik, F.T. Short, M. Waycott and S.L. Williams. 2006. A global crisis for seagrass ecosystems. Bioscience 56: 987–996.10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2Search in Google Scholar
Parrish, J. 1989. Fish communities of interacting shallow-water habitats in tropical oceanic regions. Mar. Ecol. Prog. Ser. 58: 143–160.10.3354/meps058143Search in Google Scholar
Ripley, B., B. Venables, D. Bates, K. Hornik, A. Gebhardt and D. Firth. 2015. Support functions and datasets for Venables and Ripley’s MASS. Package MASS. Accessed on 20 June 2015. http://cran.r-project.org/web/packages/MASS/index.html.Search in Google Scholar
Schobernd, Z.H., N.M. Bacheler, P.B. Conn and V. Trenkel. 2014. Examining the utility of alternative video monitoring metrics for indexing reef fish abundance. Can. J. Fish. Aquat. Sci. 71: 464–471.10.1139/cjfas-2013-0086Search in Google Scholar
Shulman, M.J. 1985. Recruitment of coral reef fishes: effects of distribution of predators and shelter. Ecology 66: 1056–1066.10.2307/1940565Search in Google Scholar
Smith, T.M., J.S. Hindell, G.P. Jenkins and R.M. Connolly. 2008. Edge effects on fish associated with seagrass and sand patches. Mar. Ecol. Prog. Ser. 359: 203–213.10.3354/meps07348Search in Google Scholar
Syms, C. and G.P. Jones. 2000. Disturbance, habitat structure, and the dynamics of a coral-reef fish community. Ecology 81: 2714–2729.10.1890/0012-9658(2000)081[2714:DHSATD]2.0.CO;2Search in Google Scholar
Tuya, F., M.A. Vanderklift, T. Wernberg and M.S. Thomsen. 2011. Gradients in the number of species at reef-seagrass ecotones explained by gradients in abundance. PLoS One 6: e20190.10.1371/journal.pone.0020190Search in Google Scholar
Unsworth, R.K.F. and L.C. Cullen. 2010. Recognising the necessity for Indo-Pacific seagrass conservation. Conserv. Lett. 3: 63–73.10.1111/j.1755-263X.2010.00101.xSearch in Google Scholar
Unsworth, R., P. De León, S. Garrard, J. Jompa, D. Smith and J. Bell. 2008. High connectivity of Indo-Pacific seagrass fish assemblages with mangrove and coral reef habitats. Mar. Ecol. Prog. Ser. 353: 213–224.10.3354/meps07199Search in Google Scholar
Vermaat, J.E., N.S.R. Agawin, C.M. Duarte, M.D. Fortes, N. Marbà and J.S. Uri. 1995. Meadow maintenece, growth and productivity of a mixed Philippine seagrass bed. Mar Ecol Prog Ser 124: 215–225.10.3354/meps124215Search in Google Scholar
Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, J.W. Fourqurean, K.L. Heck, Ar. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. USA 106: 12377–12381.10.1073/pnas.0905620106Search in Google Scholar
Willis, T.J., R.B. Millar and R.C. Babcock. 2000. Detection of spatial variability in relative density of fishes: comparison of visual census, angling, and baited underwater video. Mar. Ecol. Prog. Ser. 198: 249–260.10.3354/meps198249Search in Google Scholar
Worm, B., E.B. Barbier, N. Beumont, J.E. Duffy, C. Folke, B.S. Helpern, J.B.C. Jackson, H.K. Lotze, F. Micheli, S.R. Palumbi, E. Sala, K.A. Selkoe, J.J. Stachowicz and R. Watson. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science, 314: 787–790.10.1126/science.1132294Search in Google Scholar PubMed
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2017-0115).
Article note
This article is related to special issue Seagrass research in Southeast Asia, published in Botanica Marina 2018, vol. 61, issue 3.
©2018 Walter de Gruyter GmbH, Berlin/Boston
